Gene Transfer Agents: the ambiguous role of selfless viruses in genetic exchange and bacterial evolution

TY - JOUR

T1 - Gene Transfer Agents

T2 - the ambiguous role of selfless viruses in genetic exchange and bacterial evolution

AU - Fogg, Paul Christopher Michael

N1 - © 2024 The Authors.

PY - 2024/3/21

Y1 - 2024/3/21

N2 - Gene Transfer Agents (GTAs) are genetic elements derived from ancestral bacteriophages that have become domesticated by the host. GTAs are present in diverse prokaryotic organisms, where they can facilitate horizontal gene transfer under certain conditions. Unlike typical bacteriophages, GTAs do not exhibit any preference for the replication or transfer of their own genes; instead, they exhibit a remarkable capacity to package chromosomal, and sometimes extrachromosomal, DNA into virus-like capsids and disseminate it to neighbouring cells. Because GTAs resemble defective prophages, identification of novel GTAs is not trivial. Detection of candidates relies on genetic similarity to known GTAs, which has been fruitful in α-proteobacterial lineages but challenging in more distant bacteria. Here we consider several fundamental questions: What is the true prevalence of GTAs in prokaryote genomes? Given there are high costs for GTA production, what advantage do GTAs provide to the bacterial host to justify their maintenance? How is the bacterial chromosome recognized and processed for inclusion in GTA particles? This article highlights the challenges in comprehensively understanding GTAs' prevalence, function and DNA packaging method. Going forward, broad study of atypical GTAs and use of ecologically relevant conditions are required to uncover their true impact on bacterial chromosome evolution.

AB - Gene Transfer Agents (GTAs) are genetic elements derived from ancestral bacteriophages that have become domesticated by the host. GTAs are present in diverse prokaryotic organisms, where they can facilitate horizontal gene transfer under certain conditions. Unlike typical bacteriophages, GTAs do not exhibit any preference for the replication or transfer of their own genes; instead, they exhibit a remarkable capacity to package chromosomal, and sometimes extrachromosomal, DNA into virus-like capsids and disseminate it to neighbouring cells. Because GTAs resemble defective prophages, identification of novel GTAs is not trivial. Detection of candidates relies on genetic similarity to known GTAs, which has been fruitful in α-proteobacterial lineages but challenging in more distant bacteria. Here we consider several fundamental questions: What is the true prevalence of GTAs in prokaryote genomes? Given there are high costs for GTA production, what advantage do GTAs provide to the bacterial host to justify their maintenance? How is the bacterial chromosome recognized and processed for inclusion in GTA particles? This article highlights the challenges in comprehensively understanding GTAs' prevalence, function and DNA packaging method. Going forward, broad study of atypical GTAs and use of ecologically relevant conditions are required to uncover their true impact on bacterial chromosome evolution.

KW - Gene Transfer Agents

KW - Horizontal gene transfer

KW - DNA PACKAGING MOTOR

KW - bacteriophages

KW - BACTERIAL EVOLUTION

KW - viruses

U2 - 10.1111/mmi.15251

DO - 10.1111/mmi.15251

M3 - Review article

SN - 0950-382X

JO - Molecular Microbiology

JF - Molecular Microbiology

ER -